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Michael E. Ivan, Michael M. Safaee, Nikolay L. Martirosyan, Ana Rodríguez-Hernández, Barbara Sullinger, Priyanka Kuruppu, Julian Habdank-Kolaczkowski and Michael T. Lawton

OBJECTIVE

Anterior communicating artery (ACoA) aneurysms are common intracranial aneurysms. Despite advances in endovascular therapy, microsurgical clipping remains an important treatment for aneurysms with broad necks, large size, intraluminal thrombus, complex branches, or previous coiling. Anatomical triangles identify safe corridors for aneurysm access. The authors introduce the A1-A2 junctional triangle and the A1-A1 precommunicating triangle and examine relationships between dome projection, triangular corridors of access, and surgical outcomes.

METHODS

Preoperative catheter and CT angiograms were evaluated to characterize aneurysm dome projection. Aneurysm projection was categorized into quadrants and octants. Preoperative, intraoperative, and postoperative factors were correlated to aneurysm dome projection and patient outcomes using univariate and multivariate analyses.

RESULTS

A total of 513 patients with microsurgically treated ACoA aneurysms were identified over a 13-year period, and 400 had adequate imaging and follow-up data for inclusion. Surgical clipping was performed on 271 ruptured and 129 unruptured aneurysms. Good outcomes were observed in 91% of patients with unruptured aneurysms and 86% of those with ruptured aneurysms, with a mortality rate < 1% among patients with unruptured aneurysms. Increasing age (p < 0.01), larger aneurysm size (p = 0.03), and worse preoperative modified Rankin Scale score (p < 0.01) affected outcomes adversely. Aneurysms projecting superiorly and posteriorly required dissection in the junctional triangle, and multivariate analysis demonstrated worse clinical outcomes in these patients (p < 0.01).

CONCLUSIONS

Anteriorly and inferiorly projecting aneurysms involve only the precommunicating triangle, are simpler to treat microsurgically, and have more favorable outcomes. Superior and posterior dome projections make ACoA aneurysms more difficult to visualize and require opening the junctional triangle. Added visualization through the junctional triangle is recommended for these aneurysms in order to facilitate dissection of efferent branch arteries, careful clip application, and perforator preservation. Dome projection can be determined preoperatively from images and can help anticipate dissection routes through the junctional triangle.

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Tyler S. Cole, Sirin Gandhi, Justin R. Mascitelli, Douglas Hardesty, Claudio Cavallo and Michael T. Lawton

Venous interruption through surgical clip ligation is the gold standard treatment for ethmoidal dural arteriovenous fistula (e-dAVF). Their malignant natural history is attributable to the higher predilection for retrograde cortical venous drainage. This video illustrates an e-dAVF in a 70-year-old man with progressive tinnitus and headache. Angiogram revealed bilateral e-dAVFs (Borden III–Cognard III) with one fistula draining into cavernous sinus and another to the sagittal sinus. A bifrontal craniotomy was utilized for venous interruption of both e-dAVFs. Postoperative angiography confirmed curative obliteration with no postoperative anosmia. Bilateral e-dAVFs are rare but can be safely treated simultaneously through a single craniotomy.

The video can be found here: https://youtu.be/666edwKHGKc.

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Thomas K. Mattingly and Stephen P. Lownie

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Peyton L. Nisson, Salman A. Fard, Christina M. Walter, Cameron M. Johnstone, Michael A. Mooney, Ali Tayebi Meybodi, Michael Lang, Helen Kim, Heidi Jahnke, Denise J. Roe, Travis M. Dumont, G. Michael Lemole Jr., Robert F. Spetzler and Michael T. Lawton

OBJECTIVE

The objective of this study was to evaluate the existing Spetzler-Martin (SM), Spetzler-Ponce (SP), and Lawton-Young (LY) grading systems for cerebellar arteriovenous malformations (AVMs) and to propose a new grading system to estimate the risks associated with these lesions.

METHODS

Data for patients with cerebellar AVMs treated microsurgically in two tertiary medical centers were retrospectively reviewed. Data from patients at institution 1 were collected from September 1999 to February 2013, and at institution 2 from October 2008 to October 2015. Patient outcomes were classified as favorable (modified Rankin Scale [mRS] score 0–2) or poor (mRS score 3–6) at the time of discharge. Using chi-square and logistic regression analysis, variables associated with poor outcomes were assigned risk points to design the proposed grading system. The proposed system included neurological status prior to treatment (poor, +2 points), emergency surgery (+1 point), age > 60 years (+1 point), and deep venous drainage (deep, +1 point). Risk point totals of 0–1 comprised grade 1, 2–3 grade 2, and 4–5 grade 3.

RESULTS

A total of 125 cerebellar AVMs of 1328 brain AVMs were reviewed in 125 patients, 120 of which were treated microsurgically and included in the study. With our proposed grading system, we found poor outcomes differed significantly between each grade (p < 0.001), while with the SM, SP, and LY grading systems they did not (p = 0.22, p = 0.25, and p = 1, respectively). Logistic regression revealed grade 2 had 3.3 times the risk of experiencing a poor outcome (p = 0.008), while grade 3 had 9.9 times the risk (p < 0.001). The proposed grading system demonstrated a superior level of predictive accuracy (area under the receiver operating characteristic curve [AUROC] of 0.72) compared with the SM, SP, and LY grading systems (AUROC of 0.61, 0.57, and 0.51, respectively).

CONCLUSIONS

The authors propose a novel grading system for cerebellar AVMs based on emergency surgery, venous drainage, preoperative neurological status, and age that provides a superior prognostication power than the formerly proposed SM, SP, and LY grading systems. This grading system is clinically predictive of patient outcomes and can be used to better guide vascular neurosurgeons in clinical decision-making.

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Jan-Karl Burkhardt, Michelle H. Chua, Ethan A. Winkler, W. Caleb Rutledge and Michael T. Lawton

OBJECTIVE

During the microsurgical clipping of known aneurysms, angiographically occult (AO) aneurysms are sometimes found and treated simultaneously to prevent their growth and protect the patient from future rupture or reoperation. The authors analyzed the incidence, treatment, and outcomes associated with AO aneurysms to determine whether limited surgical exploration around the known aneurysm was safe and justified given the known limitations of diagnostic angiography.

METHODS

An AO aneurysm was defined as a saccular aneurysm detected using the operative microscope during dissection of a known aneurysm, and not detected on preoperative catheter angiography. A prospective database was retrospectively reviewed to identify patients with AO aneurysms treated microsurgically over a 20-year period.

RESULTS

One hundred fifteen AO aneurysms (4.0%) were identified during 2867 distinct craniotomies for aneurysm clipping. The most common locations for AO aneurysms were the middle cerebral artery (60 aneurysms, 54.1%) and the anterior cerebral artery (20 aneurysms, 18.0%). Fifty-six AO aneurysms (50.5%) were located on the same artery as the known saccular aneurysm. Most AO aneurysms (95.5%) were clipped and there was no attributed morbidity. The most common causes of failed angiographic detection were superimposition of a large aneurysm (type 1, 30.6%), a small aneurysm (type 2, 18.9%), or an adjacent normal artery (type 3, 36.9%). Multivariate analysis identified multiple known aneurysms (odds ratio [OR] 3.45, 95% confidence interval [CI] 2.16–5.49, p < 0.0001) and young age (OR 0.981, 95% CI 0.965–0.997, p = 0.0226) as independent predictors of AO aneurysms.

CONCLUSIONS

Meticulous inspection of common aneurysm sites within the surgical field will identify AO aneurysms during microsurgical dissection of another known aneurysm. Simultaneous identification and treatment of these additional undiagnosed aneurysms can spare patients later rupture or reoperation, particularly in those with multiple known aneurysms and a history of subarachnoid hemorrhage. Limited microsurgical exploration around a known aneurysm can be performed safely without additional morbidity.

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R. Michael Scott and Edward R. Smith

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Ali Tayebi Meybodi, Leandro Borba Moreira, Michael T. Lawton, Jennifer M. Eschbacher, Evgenii G. Belykh, Michelle M. Felicella and Mark C. Preul

OBJECTIVE

In the current neurosurgical and anatomical literature, the intracanalicular segment of the ophthalmic artery (OphA) is usually described to be within the optic nerve dural sheath (ONDS), implying direct contact between the nerve and the artery inside the optic canal. In the present study, the authors sought to clarify the exact relationship between the OphA and ONDS.

METHODS

Ten cadaveric heads were subjected to endoscopic endonasal and transcranial exposures of the OphA in the optic canal (5 for each approach). The relationship between the OphA and ONDS was assessed. Histological examination of one specimen of the optic nerve and the accompanying OphA was also performed to confirm the relationship with the ONDS.

RESULTS

In all specimens, the OphA coursed between the two layers of the dura (endosteal and meningeal) and was not in direct contact with the optic nerve, except for the first few millimeters of the proximal optic canal before it pierced the ONDS. Upon reaching the orbit, the two layers of the dura separated and allowed the OphA to literally float within the orbital fat. The meningeal dura continued as the ONDS, whereas the endosteal dura became the periorbita.

CONCLUSIONS

This study clarifies the interdural course of the OphA within the optic canal. This anatomical nuance has important neurosurgical implications regarding safe exposure and manipulation of the OphA.

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Ali Tayebi Meybodi, Leandro Borba Moreira, Andrew S. Little, Michael T. Lawton and Mark C. Preul

OBJECTIVE

Endoscopic endonasal approaches (EEAs) are increasingly being incorporated into the neurosurgeon’s armamentarium for treatment of various pathologies, including paraclinoid aneurysms. However, few anatomical assessments have been performed on the use of EEA for this purpose. The aim of the present study was to provide a comprehensive anatomical assessment of the EEA for the treatment of paraclinoid aneurysms.

METHODS

Five cadaveric heads underwent an endonasal transplanum-transtuberculum approach to expose the paraclinoid area. The feasibility of obtaining proximal and distal internal carotid artery (ICA) control as well as the topographic location of the origin of the ophthalmic artery (OphA) relative to dural landmarks were assessed. Limitations of the EEA in exposing the supraclinoid ICA were also recorded to identify favorable paraclinoid ICA aneurysm projections for EEA.

RESULTS

The extracavernous paraclival and clinoidal ICAs were favorable segments for establishing proximal control. Clipping the extracavernous ICA risked injury to the trigeminal and abducens nerves, whereas clipping the clinoidal segment put the oculomotor nerve at risk. The OphA origin was found within 4 mm of the medial opticocarotid point on a line connecting the midtubercular recess point to the medial vertex of the lateral opticocarotid recess. An average 7.2-mm length of the supraclinoid ICA could be safely clipped for distal control. Assessments showed that small superiorly or medially projecting aneurysms were favorable candidates for clipping via EEA.

CONCLUSIONS

When used for paraclinoid aneurysms, the EEA carries certain risks to adjacent neurovascular structures during proximal control, dural opening, and distal control. While some authors have promoted this approach as feasible, this work demonstrates that it has significant limitations and may only be appropriate in highly selected cases that are not amenable to coiling or clipping. Further clinical experience with this approach helps to delineate its risks and benefits.

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Gyang Markus Bot, Jan-Karl Burkhardt, Nalin Gupta and Michael T. Lawton

OBJECTIVE

Revascularization is indicated in the management of moyamoya disease (MMD), with options that include direct and indirect techniques. Indirect bypass is popular in young children because the diminutive caliber of donors and recipients makes direct bypass difficult. The authors reviewed a series of patients treated with direct superficial temporal artery (STA)–to–middle cerebral artery (MCA) bypass in combination with encephalomyosynangiosis (EMS) in children 3 years or younger to demonstrate feasibility and safety.

METHODS

A retrospective review of all surgeries for MMD over a 19-year period identified 11 procedures in 6 patients. Surgical results, angiographic outcomes, and clinical outcomes were analyzed.

RESULTS

Patients had a mean age of 22.4 months. The symptomatic hemisphere was revascularized first, and the contralateral hemisphere was revascularized on average 2.8 months later in 5 patients. All direct bypasses were patent postoperatively and remained patent at late follow-up (mean 4.1 years), with both STA and MCA diameters increasing significantly (n = 5, p < 0.03). At last follow-up (mean follow-up duration, 5.0 years), favorable outcomes (modified Rankin Scale scores 0–2) were observed in 5 of the 6 patients (83%), with 1 dependent patient remaining unchanged postoperatively.

CONCLUSIONS

Direct STA-MCA bypass in combination with EMS for MMD is feasible and safe in patients 3 years or younger, based on favorable clinical and radiological outcomes in this patient cohort. Direct bypass should be considered when immediate revascularization is needed, without the biological delay associated with indirect bypass.

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Justin R. Mascitelli, Seungwon Yoon, Tyler S. Cole, Helen Kim and Michael T. Lawton

OBJECTIVE

Although numerous arteriovenous malformation (AVM) grading scales consider eloquence in risk assessment, none differentiate the types of eloquence. The purpose of this study was to determine if eloquence subtype affects clinical outcome.

METHODS

This is a retrospective review of a prospectively collected clinical database of brain AVMs treated with microsurgery in the period from 1997 to 2017. The only inclusion criterion for this study was the presence of eloquence as defined by the Spetzler-Martin grading scale. Eloquence was preoperatively categorized by radiologists. Poor outcome was defined as a modified Rankin Scale (mRS) score 3–6, and worsening clinical status was defined as an increase in the mRS score at follow-up. Logistic regression analyses were performed.

RESULTS

Two hundred forty-one patients (49.4% female; average age 33.9 years) with eloquent brain AVMs were included in this review. Of the AVMs (average size 2.7 cm), 54.4% presented with hemorrhage, 46.2% had deep venous drainage, and 17.0% were diffuse. The most common eloquence type was sensorimotor (46.1%), followed by visual (27.0%) and language (22.0%). Treatments included microsurgery alone (32.8%), microsurgery plus embolization (51.9%), microsurgery plus radiosurgery (7.9%), and all three modalities (7.5%). Motor mapping was used in 9% of sensorimotor AVM cases, and awake speech mapping was used in 13.2% of AVMs with language eloquence. Complications occurred in 24 patients (10%). At the last follow-up (average 24 months), 71.4% of the patients were unchanged or improved and 16.6% had a poor outcome. There was no statistically significant difference in the baseline patient and AVM characteristics among the different subtypes of eloquence. In a multivariate analysis, in comparison to visual eloquence, both sensorimotor (OR 7.4, p = 0.004) and language (OR 6.5, p = 0.015) eloquence were associated with poor outcomes. Additionally, older age (OR 1.31, p = 0.016) and larger AVM size (OR 1.37, p = 0.034) were associated with poor outcomes.

CONCLUSIONS

Unlike visual eloquence, sensorimotor and language eloquence were associated with worse clinical outcomes after the resection of eloquent AVMs. This nuance in AVM eloquence demands consideration before deciding on microsurgical intervention, especially when numerical grading systems produce a score near the borderline between operative and nonoperative management.